Introduced Siberian Chipmunks (Tamias sibiricus barberi) Contribute More to Lyme Borreliosis Risk than Native Reservoir Rodents

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Marsot, Maud ^a,b   Chapuis, Jean Louis ^b   Gasqui, Patrick ^a   Dozières, Anne ^b   Masséglia, Sébastien ^a   Pisanu, Benoit ^b   Ferquel, Elisabeth ^c   Vourc'h, Gwenaël ^a  

^a EPIA   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APODEMUS SYLVATICUS; ARTICLE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA GARINII; CONTROLLED STUDY; DISEASE TRANSMISSION; HOST PATHOGEN INTERACTION; INFECTION RISK; IXODES RICINUS; LYME DISEASE; MYODES GLAREOLUS; NONHUMAN; NYMPH; PARASITE LOAD; PREVALENCE; RODENT; SEASONAL VARIATION; SPECIES COMPARISON; SPECIES COMPOSITION; SPECIES DIVERSITY; SPECIES INTRODUCTION; TAMIAS; TAMIAS SIBIRICUS BARBERI; TICK BITE; TICK INFESTATION; VOLE; ZOONOSIS;

ANIMALS; ARVICOLINAE; BORRELIA BURGDORFERI; DISEASE RESERVOIRS; DNA PRIMERS; FRANCE; INTRODUCED SPECIES; IXODES; LYME DISEASE; MICE; MURINAE; POLYMERASE CHAIN REACTION; POPULATION DENSITY; PREVALENCE; RNA, RIBOSOMAL, 16S; SCIURIDAE; TICK INFESTATIONS;

EID: 84873197091     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055377     Document Type: Article

References (61)

1. Vourc'h G, Plantard O, Morand S (2012) How does biodiversity influence the ecology of infectious disease? In: Springer, editor. New frontiers of molecular epidemiology of infectious diseases. 291-309.
2. Keesing F, Holt RD, Ostfeld RS, (2006) Effects of species diversity on disease risk. Ecology Letters 9: 485-498.
3. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK, (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8: 1468-1473.
4. Hartemink NA, Randolph SE, Davis SA, Heesterbeek JAP, (2008) The basic reproduction number for complex disease systems: Defining R0 for tick-borne infections. American Naturalist 171: 743-754.
5. Randolph SE, Craine NG, (1995) General framework for comparative quantitative studies on transmission of tick-borne diseases using Lyme Borreliosis in Europe as an example. Journal of Medical Entomology 32: 765-777.
6. Brisson D, Dykhuizen DE, Ostfeld RS, (2007) Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proceedings of the Royal Society B-Biological Sciences 101: 1175-1180.
7. Mather TN, Wilson ML, Moore SI, Ribeiro JM, Spielman A, (1989) Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). American Journal of Epidemiology 130: 143-150.
8. Walther GR, Roques A, Hulme PE, Sykes MT, Pysek P, et al. (2009) Alien species in a warmer world: risks and opportunities. Trends in Ecology & Evolution 24: 686-693.
9. Daszak P, Cunningham AA, Hyatt AD, (2000) Emerging infectious diseases of wildlife- Threats to biodiversity and human health. Science 289: 1756-1756.
10. Atkinson CT, LaPointe DA, (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery 23: 53-63.
11. Kozubikova E, Filipova L, Kozak P, Duris Z, Martin MP, et al. (2009) Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conservation Biology 23: 1204-1213.
12. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM, (2009) Parasite spillback: A neglected concept in invasion ecology? Ecology 90: 2047-2056.
13. O'Brien VA, Moore AT, Young GR, Komar N, Reisen WK, et al. (2011) An enzootic vector-borne virus is amplified at epizootic levels by an invasive avian host. Proceedings of the Royal Society B-Biological Sciences 278: 239-246.
14. Obolenskaya EV, Lee MY, Dokuchaev NE, Oshida T, Lee MS, et al. (2009) Diversity of Palaearctic chipmunks (Tamias, Sciuridae). Mammalia 73: 281-298.
15. Smith R, Takkinen J, (2006) Editorial team (2006) Lyme borreliosis: Europe-wide coordinated surveillance and action needed? Euro Surveillance 11: E060622.1.
16. Pisanu B, Obolenskaya EV, Baudry E, Lissovsky AA, Chapuis J-L (2013) Narrow phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia: Sciuridae) established in France. Biological Invasions. doi:101007/s10530-012-0375-x.
17. Chapuis J-L, (2005) Distribution in France of a naturalized pet, the Siberian chipmunk (Tamias sibiricus). Revue d'Ecologie (Terre et Vie) 60: 239-253.
18. Chapuis J-L, Obolenskaya E, Pisanu B, Lissovsky A (2011) Datasheet on Tamias sibiricus. CABI, Invasive Species Compendium, Wallingford, UK Available: http://www.cabi.org/isc/?compid=5&dsid=62788&loadmodule=datasheet&page=481&site=144. Accessed 2013 Jan 3.
19. Rizzoli A, Hauffe HC, Carpi G, Vourc'h GI, Neteler M, et al. (2011) Lyme borreliosis in Europe. Eurosurveillance 16: 2-9.
20. Hanincovà K, Schafer SM, Etti S, Sewell HS, Taragel'ovà V, et al. (2003) Association of Borrelia afzelii with rodents in Europe. Parasitology 126: 11-20.
21. Hanincovà K, Taragel'ovà V, Koci J, Schafer SM, Hails R, et al. (2003) Association of Borrelia garinii and Borrelia valaisiana with songbirds in Slovakia. Applied and Environmental Microbiology 69: 2825-2830.
22. Humair PF, Gern L, (1998) Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69: 213-227.
23. Marsot M, Sigaud M, Chapuis J-L, Ferquel E, Cornet M, et al. (2011) The introduced Siberian chipmunk (Tamias sibiricus barberi) harbours more diverse Borrelia burgdorferi sensu lato genospecies than the native bank vole. Applied and Environmental Microbiology 77: 5516-5721.
24. Pisanu B, Marsot M, Marmet J, Chapuis J-L, Reale D, et al. (2010) Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France. International Journal for Parasitology 40: 1277-1283.
25. Randolph SE, (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by Ixodid ticks as vectors. Parasitology 129: S37-S66.
26. Maresca B (2000) La fréquentation des forêts en Ile-de-France- Caractéristiques des sorties et flux de visite des franciliens. CREDOC.
27. Marmet J, Pisanu B, Chapuis J-L, (2009) Home range, range overlap, and site fidelity of introduced Siberian chipmunks in a suburban French forest. European Journal of Wildlife Research 55: 497-504.
28. Sinsky RJ, Piesman J, (1989) Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. Journal of Clinical Microbiology 27: 1723-1727.
29. Craine NG, Randolph SE, Nuttall PA, (1995) Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochete, in a British woodland. Folia Parasitologica 42: 73-80.
30. Schmidt KA, Ostfeld RS, Schauber EM, (1999) Infestation of Peromyscus leucopus and Tamias striatus by Ixodes scapularis (Acari: Ixodidae) in relation to the abundance of hosts and parasites. Journal of Medical Entomology 36: 749-757.
31. Marmet J, Pisanu B, Chapuis JL, (2011) Natal dispersal of introduced Siberian chipmunks, Tamias sibiricus, in a suburban forest. Journal of Ethology 29: 23-29.
32. Marsot M, (2008) Dynamique temporelle de l'infection des petits rongeurs par l'agent de la maladie de Lyme (Borrelia burgdorferi sl) en forêt de Sénart. Master 2, Université Claude Bernard, Lyon 1: 34.
33. Johnson NL, Kotz S, Kemp AW (1992) Univariate Discrete Distributions; Statistics WSiPaM, editor. 565 p.
34. Marconi RT, Garon CF, (1992) Development of polymerase chain reaction primer sets for diagnosis of Lyme disease and for species-specific identification of Lyme disease isolates by 16S rRNA signature nucleotide analysis. Journal of Clinical Microbiology 30: 2830-2834.
35. Postic D, Assous MV, Grimont PA, Baranton G, (1994) Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. International Journal of Systematic Bacteriology 44: 743-752.
36. Margos G, Vollmer SA, Cornet M, Garnier M, Fingerle V, et al. (2009) A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Applied and Environmental Microbiology 75: 5410-5416.
37. Marmet J (2008) Traits d'histoire de vie du Tamia de Sibérie Tamias sibiricus, espèce exotique naturalisée dans la forêt de Sénart (Essonne): démographie, biologie de la reproduction, occupation de l'espace et dispersion. Muséum National d'Histoire Naturelle, Paris. 172 p.
38. Paterson S, Lello J, (2003) Mixed models: getting the best use of parasitological data. Trends in Parasitology 19: 370-375.
39. Efford MG (2012) secr: Spatially explicit capture-recapture models. R package version 2.3.2. Available: http://CRAN.R-project.org/package=secr. Accessed 2013 Jan 3.
40. Telfer S, Bown K, (2012) The effects of invasion on parasite dynamics and communities. Functional Ecology 26: 1288-1299.
41. Efford MG, Dawson DK, Borchers DL, (2009) Population density estimated from locations of individuals on a passive detector array. Ecology 90: 2676-2682.
42. Pisanu B, Marmet J, Beaucournu JC, Chapuis JL, (2008) Fleas community in introduced Siberian chipmunks (Tamias sibiricus Laxmann) in forest of Senart, France. Parasite 15: 35-43.
43. Vourc'h G, Marmet J, Chassagne M, Bord S, Chapuis J-L, (2007) Borrelia burgdorferi sensu lato in Siberian chipmunks (Tamias sibiricus) introduced in suburban forests in France. Vector-Borne and Zoonotic Diseases 7: 637-641.
44. Pollock KH, Otto MC, (1983) Robust estimation of population size in closed animal populations from capture-recapture experiments. Biometrics 39: 1035-1049.
45. Rexstad E, Burnham K (1992) User's guide for interactive program CAPTURE: Fort Collins: Colorado Cooperative Fish and Wildlife Research Unit.
46. Brown LE, (1956) Movements of some British small mammals. Journal of Animal Ecology 25: 54-71.
47. Kikkawa J, (1964) Movement, activity and distribution of the small rodents Chlethrionomys glareolus and Apodemus sylvaticus in woodland. Journal of Animal Ecology 33: 259-299.
48. Radda A, (1968) Populations studien an Rotelmausen (Clethrionomys glareolus Schreber, 1780) durch Markierungsfang in Niederosterreich. Oecologia 1: 219-235.
49. McCullagh P, Nelder JA (1989) Generalized Linear Models; Hall/CRC C, editor. London.
50. Gern L, Estrada-Peña A, Frandsen F, Gray J, Jaenson T, et al. (1998) European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt für Bakteriologie 287: 196-204.
51. Humair PF, Rais O, Gern L, (1999) Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 118: 33-42.
52. McLean R, Ubico SR, Cooksey LM, (1993) Experimental infection of the Eastern chipmunk (Tamias striatus) with the Lyme disease spirochete (Borrelia burgdorferi). Journal of Wildlife Diseases 29: 527-532.
53. Matuschka FR, Richter D, Fischer P, Spielman A, (1990) Time of repletion of subadult Ixodes ricinus ticks feeding on diverse hosts. Parasitology Research 76: 540-544.
54. Randolph SE, Dobson A, (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139: 847-863.
55. Humair PF, Peter O, Wallich R, Gern L, (1995) Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. Journal of Medical Entomology 32: 433-438.
56. Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, et al. (2004) An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences of the United States of America 101: 18159-18164.
57. Kurtenbach K, Peacey M, Rijpkema SGT, Hoodless AN, Nuttall PA, et al. (1998) Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64: 1169-1174.
58. Kybicova K, Kurzova Z, Hulinska D, (2008) Molecular and serological evidence of Borrelia burgdorferi sensu lato in wild rodents in the Czech Republic. Vector Borne and Zoonotic Diseases 8: 645-652.
59. Paulauskas A, Arnbrasiene D, Radzijevskaja J, Rosef O, Turcinaviciene J, (2008) Diversity in prevalence and genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in Lithuania and Norway. International Journal of Medical Microbiology 298 S1: 180-187.
60. Dorn W, Messutat S, Kipp S, Sunder U, Feldman A, et al. (1999) Seasonal variation in the infestation of rodents with Ixodes ricinus (Acari: Ixodidae) and prevalence of infection with Borrelia burgdorferi in a recreation area. Proceedings of the 3rd International Conference on Urban Pests. Czech University of Agriculture, Prague, Czech Republic, 19-22 July 1999: 463-469.
61. Tälleklint L, Jaenson TGT, (1997) Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden. Experimental and Applied Acarology 21: 755-771.